LETTERS

Alaria alata neuroretinitis (3), to severe-to-lethal that described gross lesions produced anaphylactic shock caused by larva by A. alata trematodes (6,8), to our Infection in migrans (4,5). The genus has 7 knowledge, no data have been pub- European Mink species; only A. alata is found natural- lished concerning lesions produced by ly in Europe (6), a species which has natural infection in nonhuman hosts. To the Editor. Alariosis is a re- not thus far been shown to be respon- Our report provides a detailed descrip- emerging zoonotic disease caused by sible for human infections. tion of the lesions, shown by micros- infection with larval stages of trema- A. alata infection is common in copy, which suggests the pathogenic todes of the genus Alaria. The trema- its typical definitive host (red fox, mechanisms. todes are found in wildlife that inhabit Vulpes vulpes) and in certain paratenic One adult female European mink wetlands, and these may serve hosts (wild boar, Sus scrofa) (1). How- (Mustela lutreola) was found dead dur- as possible reservoirs for these organ- ever, the role of other paratenic hosts ing standard surveillance operations in isms that cause human infection (1). is poorly known. Among these, mus- which box traps were used; this trap- The main sources for human infection telids are reported to harbor mesocer- ping was part of biodiversity and ecol- are suids and frogs (1). In humans, the cariae of A. alata trematodes (7). The ogy studies in the central part of the clinical features of alariosis caused pathogenic effect of A. alata infection Danube delta in Romania (45°08′ N, by infections with the North Ameri- has been poorly studied, because most 29°19′E) in March 2010. The corpse can species of Alaria vary from mild lesions described were in humans in- was deep-frozen and analyzed after 3 and asymptomatic to moderate with fected with other species of Alaria. months in the laboratory. During nec- respiratory or cutaneous signs (2) or Except for 2 experimental studies ropsy, multiple, well-defined, whitish

Figure. Lesions produced by mesocercariae of Alaria alata in European mink. A) Mesocercariae in the muscle and subcutaneous tissue produce whitish, round or slightly oval, well-defined nodules. B) Free mesocercarium after artificial digestion, showing the characteristics of A. alata mesocercarium: piriform body with anterior oral sucker (OS), acetabulum (AC) positioned in the center of the parasite, 2 pairs of large, finely granulated penetration glands (white stars), limiting the anterior part of the acetabulum, linear ducts of penetration glands (DPG) converging to the oral opening of the oral sucker and large double ceca placed posterior to the acetabulum. C) Histologic section showing an encysted mesocercarium in the muscle (parasite is surrounded by a capsule and pericystic inflammation, which extends to the surrounding muscular tissue). D) Mononuclear leucocytes (arrowheads) scattered between the fibroblastic proliferations (white arrows) and collagen deposits (black stars). Muscle fibers are atrophic due to compression (black arrows). E) Microscopic detail of the inset from panel C. Some mesocercariae (indicated by black arrow) are enclosed in a thin, pale staining capsule (white arrows). Note the lack of leukocyte response. F) Migration route of the parasite (route with center marked by the black star), followed by invasion of nonnecrotic muscle fibers by mononucleate inflammatory cells (white arrow) located mainly in the center of the migration tract and fibrous connective tissue with collagen fibers densely packed at the periphery (black arrows) and more loosely in the center (arrowheads). Hematoxylin–eosin stain (panels C, D, E); Masson trichrome (panel F); original magnifications x40 (panels B and C), x200 (panels D and F), and x400 (panel E). A color version of this figure is available online (wwwnc.cdc.gov/EID/article/19/09/13-0081-F1.htm).

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 19, No. 9, September 2013 1547 LETTERS nodules were observed in most muscu- A. alata infection in its paratenic host Cluj-Napoca, Cluj-Napoca, Romania (F. lar and subcutaneous tissues (Figure, appears to be caused by mesocercarial Tăbăran, A.D. Sándor, C. Cătoi, A.D. panel A), with no evident preferential migration. This view is sustained by Mihalca); and Danube Delta National Insti- localization. We collected samples the presence of mononuclear cells that tute for Research and Development, Tul- from these tissues for artificial diges- it infiltrates and by the appearance of cea, Romania (M. Marinov) tion (9,10) and histologic examination, the granulomatous tissue in various DOI: http://dx.doi.org/10.3201/eid1909.130081 using the routine paraffin-embedding stages of maturation, which leads to protocol and the following staining muscle and subcutaneous fibroplasia. References methods: hematoxylin-eosin, Masson The reparatory nature of the lesions trichrome, and Gordon and Sweet. suggests that the inflammation is prob- 1. Möhl K, Grosse K, Hamedy A, Wüste T, Artificial digestion released ably the result of direct tissue damage Kabelitz P, Lücker E. Biology of Alaria spp. and human exposition risk to Alaria parasites (6 larvae/5 gm tissue) with rather than an immune reaction tar- mesocercariae-a review. Parasitol Res. typical larval trematode structures geted toward the parasitic antigens. 2009;105:1–15 http://dx.doi.org/10.1007/ (Figure, panel B). By microscopy, we This assumption could explain the lo- s00436-009-1444-7. observed that morphologic features of cal absence of inflammatory reaction 2. Kramer MH, Eberhard ML, Blankenberg TA. Respiratory symptoms and subcutane- these larvae were consistent with A. around the parasites. The lack of in- ous granuloma caused by mesocercariae: alata mesocercariae (6). Histopatho- flammation was previously observed a case report. Am J Trop Med Hyg. logic examination confirmed the also with A. americana infection of 1996;55:447–8. presence of parasitic forms in muscle humans (4). The structure of all me- 3. McDonald HR, Kazacos KR, Schatz H, Johnson RN. Two cases of intraocular sections (Figure, panel C). The me- socercariae observed by microscopy infection with Alaria mesocercaria socercariae were located in the con- suggested that they were alive and ac- (). Am J Ophthalmol. 1994; nective fibrous tissue of the perimy- tive before the mink carcass was fro- 117:447–55. sium or between the muscle fibers. zen. Because no mesocercariae were 4. Fernandes BJ, Cooper JD, Cullen JB, Freeman RS, Ritchie AC, Scott AA, The typical structure of muscle fibers surrounded by adult connective tissue et al. Systemic infection with Alaria was altered around the larvae, with or by granulomatous inflammation, americana (Trematoda). Can Med Assoc inflammatory cell reactions, repre- together with the multiple presences J. 1976;115:1111–4. sented mainly by lymphocytes, mac- of migratory routes, the continuous 5. Freeman RS, Stuart PF, Cullen SJ, Ritchie AC, Mildon A, Fernandes BJ, et al. Fatal rophages, and plasma cells (Figure, mobility of the parasites through the human infection with mesocercariae of the panel D). In other areas, the inflam- host’s tissues was strongly suggested. trematode Alaria americana. Am J Trop matory reaction around the parasite Although data on the pathologic Med Hyg. 1976;25:803–7. was minimal or absent (Figure, panel changes caused by Alaria spp. in gen- 6. Skrjabin KI. editor. Trematodes of ani- mals and man; essentials of trematodol- E). In certain histologic sections, the eral, and A. alata parasites in particu- ogy, vol. XVIII. Jerusalem (Israel): Pro- damaged muscular tissue was re- lar, are scarce, the migration pattern gram for Scientific Translations; 1965. p. placed by granulation tissue in vari- and the lesions seem to be dependent 327–43. ous stages of development (Figure, on the particular parasite and host spe- 7. Anisimova EI. Study on the European mink Mustela lutreola helminthocenoses panel F). The maturity of the granu- cies. The reparatory nature of the le- in connection with the American mink lation tissue differed substantially, sions suggests that the inflammation is M. vison expansion in the Belarus: story depending on the muscular areas the result of direct tissue damage rath- of the study and review of the results. examined. Some lesions were found er than an immune reaction targeted Helminthologia. 2004;41:193–6. 8. Odening K. The “Duncker’s muscle fluke” in adult connective tissue, formed by toward the parasitic antigens. can be transmitted experimentally to mon- mature collagen scar fibers (type I keys [in German]. Monatsh Veterinarmed. collagen) and few inflammatory cells, The research was conducted with 1961;16:395–9. whereas other lesions had reticulin fi- the support of Unitatea Executivă pen- 9. Gamble HR, Bessonov AS, Cuperlovic K, Gajadhar AA, van Knapen F, Noeckler K. bers (type III collagen) with numer- tru Finantarea Învătământului Superior, a Cercetării, Dezvoltării si Inovării (UE- International Commission on Trichinello- ous inflammatory cells. The lesions sis: recommendations on methods for the of the subcutaneous connective tissue FISCDI) grant PCE236/2011. control of Trichinella in domestic and wild consisted of an inflammatory reac- animals intended for human consumption. Vet Parasitol. 2000;93:393–408. http:// tion (panniculitis). The inflammation Flaviu Tăbăran, dx.doi.org/10.1016/S0304-4017(00) was characterized by a low number of Attila David Sándor, 00354-X mononuclear leukocytes and fibrin- Mihai Marinov, Cornel Cătoi, 10. Portier J, Jouet D, Ferté H, Gibout O, ous exudate and fibroplasia. and Andrei Daniel Mihalca Heckmann A, Boireau P, et al. New data in France on the trematode Alar- The polyphasic nature of muscle Author affiliations: University of Agricul- ia alata (Goeze, 1792) obtained dur- and subcutaneous lesions produced by tural Sciences and Veterinary Medicine ing Trichinella inspections. Parasite.

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2011;18:271–5. http://dx.doi.org/10.1051/ ignored for more than 3 decades and Sheepdogs that lived in the study parasite/2011183271 then restarted in 2011 in Iran. areas were also used as sentinel ani- This study was designed to inves- mals. Blood samples were collected Address for correspondence: Attila D. Sándor, tigate plague among resident animals from 58 sheepdogs in 15 villages Department of Parasitology and Parasitic in western Iran, specificallyregion in 2011 and from 59 sheepdogs in 8 Diseases, University of Agricultural Sciences localities along the border between villages in 2012. Of 117 serum and Veterinary Medicine, Cluj-Napoca, Calea the Kurdistan and Hamadan Prov- samples analyzed, 4 (3.42%) had IgG Mănăştur 3-5, RO-400372, Cluj, Romania; inces, where plague in wildlife has titers against F1, 1 in 2011 and the email: [email protected] been repeatedly reported (enclosed other 3 in 2012 (Table). Finally, wild by 47.900° and 48.284° north latitude animals such as jackals, foxes, rabbits, and 35.4616° and 35.7829° east lon- and hedgehogs were hunted in the gitude). The epidemiologic team was study areas, and blood samples were based at the Akanlu Research Center taken immediately. None of the serum Serologic Survey of of the Pasteur Institute of Iran, in a vil- samples obtained from 3 foxes, 2 jack- Plague in Animals, lage ≈100 km from Kabudar Ahang, als, 8 rabbits, and 1 hedgehog had IgG Western Iran Hamadan Province, at an altitude of against F1 (Table). ≈1,600 m. The study was conducted Because a well-established plague To the Editor: Plague has been during June–September in 2011 and focus existed in Iranian Kurdistan, one of the most devastating infec- 2012. In 2011, a large area (2,000 km2) with cases occurring until 1978 tious diseases in human history. The was selected and, because only 1 Y. (9), complete extinction of this focus is etiologic agent, Yersinia pestis, pri- pestis–positive dog sample was found, most unlikely. Our study demonstrates marily affects rodents and is usually in 2012, , the study area was reduced that animal reservoirs (Meriones ro- transmitted to humans through infec- to 1,200 km2 and confined to locali- dents) and flea vectors (Xenopsylla tive flea bites. Endemic plague foci ties in which the Y. pestis–positive dog spp.) shown to be central to the plague result from circulation of the plague sample was identified the previous ecologic cycle in Iran still are found bacillus in its rodent reservoir, the year; 3 additional Y. pestis–positive in high numbers in a previously active source of human plague cases (1). and 1 Y. pestis–positive rodent focus. The fact that 70% of trapped ro- Carnivores such as dogs and foxes, were found in 2012. dents were infested with fleas, with an which prey on rodents and eat their The average number of traps average Xenopsylla spp. index of 4.10, fresh carcasses, are valuable sentinel used per night per locality was 13. may be considered as circumstances animals for plague serosurveillance A total of 46 rodents were entrapped most favorable for the onset of plague in disease-endemic foci, although from 26 localities in 998 traps (4.61% epizootics. Furthermore, the detection their infections are usually asymp- success) during the first year, and 52 of Y. pestis–specific IgG in 1.02% of tomatic (2,3). rodents were captured in 30 locali- trapped rodents and 3.42% of sentinel Plague epidemics have caused ties in 1,164 traps (4.46% success) dogs is highly suggestive of active loss of human life in various parts of during the second year. They were circulation of Y. pestis in its natural Iran. During 1947–1966 in western mostly members of the Meriones animal reservoir. Because Y. pestis Iran, 9 human epidemics occurred genus, although a few Microtus so- antibodies last only for ≈6 months in and caused 156 deaths. The last case cialis irani and 1 Ellobius lutescens dogs (2), seropositivity of these dogs of human plague was reported in 1966 rodents were also caught (Table). A indicates newly acquired infections. (4). Field investigations identified 4 total of 281 fleas were collected on This fact that Y. pestis–-positive Meriones rodent species as Y pestis 70.41% of trapped rodents (Table), animals were found over the 2-year reservoirs; 2 were resistant (M. per- corresponding to an average flea in- surveillance period suggests that this sicus and M. libycus), and the other dex of 4.10 for infested rodents. All area could be an active plague focus. 2 (M. tristrami and M. vinogradovi) fleas were Xenopsylla spp. ELISA Therefore, although no official re- were susceptible to death from infec- was performed as described (7) to ports of human plague in Iran have tion (4,5). The epidemiologic inves- detect antibodies against Y. pestis F1 been made since 1966, this study in- tigations demonstrated a 3–4 year capsular antigen. Samples positive by dicates that the epidemiologic condi- plague epizootic cycle in Iran (5). ELISA were confirmed by using the tions needed to trigger an outbreak The last official report of plague in inhibition ELISA method (8). Of 98 have been met. It is thus of utmost rodents in Iran dates back to 1978, in trapped rodents, 1 (1.02%) had IgG importance to maintain and strengthen Sarab County in the East Azarbaijan against F1 (Table), an M. persicus the health system with plague surveil- Province (6). Plague surveillance was jird caught in 2012. lance in western Iran.

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